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Abstract Antagonist interactions, such as predator-prey interactions, are widespread in nature and drive both ecological and evolutionary outcomes. Coevolutionary outcomes of antagonistic interactions have been shown to be influenced by environmental conditions, yet the role of abiotic stress in modifying these outcomes remains insufficiently understood. Here we explored how the addition of temperature stress altered evolutionary trajectories of traits of both species in the Pseudomonas fluorescens – Tetrahymena pyriformis (bacteria- ciliate) predator prey system. We found that temperature stress impeded the evolution of traits important for antagonistic interactions in both species. Prey defense levels as well as predators’ ability to eat prey were limited under temperature stress. We also found that the addition of temperature stress altered growth rate evolution in evolving populations of both species. Taken together, our results show that temperature stress not only alters the evolutionary trajectories of both predator and prey traits but also hinders their coevolution. These findings suggest that environmental stressors may weaken reciprocal coevolution which could have important consequences for the stability and persistence of ecological communities. 

Road salt application improves road safety but leads to salinization of nearby freshwater ecosystems. If populations readily adapt to their local salinity environment, then we expect to find differences in salt tolerance between populations found near vs. far from roads. We determined the salt tolerance of 10 wild strains of the freshwater microbial eukaryote Tetrahymena. We found no significant correlation between salt tolerance and road distance, suggesting that these populations are not locally adapted to their salinity environment. This result may be due to the unexpectedly high salt tolerance across lines, unknown patterns of migration between ponds, or sampling conditions. 

ABSTRACT Humans are changing habitat for wildlife in myriad ways and for populations to persist, they must adapt to this change. In parts of the world that experience snow and ice, road salts are often used to make driving safer in the winter. Runoff from these roads increases the salinity in nearby bodies of water, which has been shown to have detrimental physiological and ecological effects in freshwater ecosystems; however, the evolutionary consequences of salinization remain unclear.Tetrahymenaare microbial eukaryotes that live in freshwater habitats and serve as an important link in the microbial food loop. In this study, we tested howT. thermophilacan evolve in response to increasing concentrations of road salts in their environment. Using experimental evolution, we found thatT. thermophilapopulations adapted to survive and grow in concentrations of up to 18 g/L of NaCl and 17 g/L MgCl₂, approximately twice the salinity tolerance of ancestral populations. However, populations adapted to the highest salt concentrations experience fitness trade‐offs of reduced survival and growth rate and longer lag times when grown in salt‐free environments. These results demonstrate the rapidity with which microbial populations can respond to anthropogenic changes to their environment, yet highlight the potential costs associated with this adaptation. 

Abstract Correlated responses to selection have long been observed and studied; however, it remains unclear when they will arise, and in what direction. To contribute to a growing understanding of correlated responses to selection, we used experimental evolution of the ciliateTetrahymena thermophilato study direct and correlated responses in a variety of different environmental conditions. One experiment focused on adaptation to two different temperatures and the correlated responses across temperatures. Another experiment used inhibitory concentrations of a variety of compounds to test direct and correlated responses to selection. We found that all populations adapted to the environments in which they evolved. We also found many cases of correlated evolution across environments; few conditions resulted in trade‐offs and many resulted in a positive correlated response. Surprisingly, in many instances, the correlated response was of a larger magnitude than the direct response. We find that ancestral fitness predicts the extent of adaptation, consistent with diminishing returns epistasis. Unexpectedly, we also find that this pattern of diminishing returns holds across environments regardless of the environment in which evolution occurs. We also found that the correlated response is asymmetric across environments, that is, the fitness of a population evolved in one environment and assayed in a second was inversely related to the fitness of a population evolved in the second environment and assayed in the first. These results support the notion that positive correlated responses to selection across environments are frequent, and worth further study. 

Colpoda, one of the most widespread ciliated protozoa in soil, are poorly understood in regard to their genetics and evolution. Our research revealed extreme mitochondrial gene rearrangements dominated by gene loss events, potentially leading to the streamlining ofColpodamitogenomes. Surprisingly, while interspecific rearrangements abound, our population-level mitogenomic study revealed a conserved gene order within species, offering a potential new identification criterion. Phylogenomic analysis traced their lineage over 326 million years, revealing two distinct groups. Substantial genomic divergence might be associated with the lack of extended collinear blocks and relaxed purifying selection. This study systematically revealsColpodaciliate mitogenome structures and evolution, providing insights into the survival and evolution of these vital soil microorganisms. 

ABSTRACT <p>Microorganisms play a central role in sustaining soil ecosystems and agriculture, and these functions are usually associated with their complex life history. Yet, the regulation and evolution of life history have remained enigmatic and poorly understood, especially in protozoa, the third most abundant group of organisms in the soil. Here, we explore the life history of a cosmopolitan species—<italic>Colpoda steinii</italic>. Our analysis has yielded a high-quality macronuclear genome for<italic>C. steinii</italic>, with size of 155 Mbp and 37,123 protein-coding genes, as well as mean intron length of ~93 bp, longer than most other studied ciliates. Notably, we identify two possible whole-genome duplication events in<italic>C. steinii</italic>, which may account for its genome being about twice the size of<italic>C. inflata’s</italic>, another co-existing species. We further resolve the gene expression profiles in diverse life stages of<italic>C. steinii</italic>, which are also corroborated in<italic>C. inflata</italic>. During the resting cyst stage, genes associated with cell death and vacuole formation are upregulated, and translation-related genes are downregulated. While the translation-related genes are upregulated during the excystment of resting cysts. Reproductive cysts exhibit a significant reduction in cell adhesion. We also demonstrate that most genes expressed in specific life stages are under strong purifying selection. This study offers a deeper understanding of the life history evolution that underpins the extraordinary success and ecological functions of microorganisms in soil ecosystems.</p><sec><title>IMPORTANCEColpodaspecies, as a prominent group among the most widely distributed and abundant soil microorganisms, play a crucial role in sustaining soil ecosystems and promoting plant growth. This investigation reveals their exceptional macronuclear genomic features, including significantly large genome size, long introns, and numerous gene duplications. The gene expression profiles and the specific biological functions associated with the transitions between various life stages are also elucidated. The vast majority of genes linked to life stage transitions are subject to strong purifying selection, as inferred from multiple natural strains newly isolated and deeply sequenced. This substantiates the enduring and conservative nature ofColpoda’s life history, which has persisted throughout the extensive evolutionary history of these highly successful protozoa in soil. These findings shed light on the evolutionary dynamics of microbial eukaryotes in the ever-fluctuating soil environments. This integrative research represents a significant advancement in understanding the life histories of these understudied single-celled eukaryotes. 

Abstract Understanding the mechanisms that generate genetic variation, and thus contribute to the process of adaptation, is a major goal of evolutionary biology. Mutation and genetic exchange have been well studied as mechanisms to generate genetic variation. However, there are additional factors, such as genome architecture, that may also impact the amount of genetic variation in some populations, and the extent to which these variation generating mechanisms are themselves shaped by natural selection is still an open question. To test the effect of genome architecture on the generation of genetic variation, and hence evolvability, we studied Tetrahymena thermophila, a ciliate with an unusual genome structure and mechanism of nuclear division, called amitosis, whereby homologous chromosomes are randomly distributed to daughter cells. Amitosis leads to genetic variation among the asexual descendants of a newly produced sexual progeny because different progeny cells will contain different combinations of parental alleles. We hypothesize that amitosis thus increases the evolvability of newly produced sexual progeny relative to their unmated parents and species that undergo mitosis. To test this hypothesis, we used experimental evolution and simulations to compare the rate of adaptation in T. thermophila populations founded by a single sexual progeny to parental populations that had not had sex in many generations. The populations founded by a sexual progeny adapted more quickly than parental populations in both laboratory populations and simulated populations. This suggests that the additional genetic variation generated by amitosis of a heterozygote can increase the rate of adaptation following sex and may help explain the evolutionary success of the unusual genetic architecture of Tetrahymena and ciliates more generally. 

Experimental evolution has provided novel insight into a wide array of biological processes. Species in the genus Tetrahymena are proving to be a highly useful system for studying a range of questions using experimental evolution. Their unusual genomic architecture, diversity of life history traits, importance as both predator and prey, and amenability to laboratory culture allow them to be studied in a variety of contexts. In this paper, we review what we are learning from experimental evolution with Tetrahymena about mutation, adaptation, and eco-evolutionary dynamics. We predict that future experimental evolution studies using Tetrahyemena will continue to shed new light on these processes.